Environ. Sci. Technol.
1999, 33, 469-475
Phytoremediation of
Radiocesium-Contaminated Soil in
the Vicinity of Chernobyl, Ukraine
S L A V I K D U S H E N K O V , * ,†
ALEXANDER MIKHEEV,‡
ALEXEI PROKHNEVSKY,‡
MICHAEL RUCHKO,‡ AND
BORIS SOROCHINSKY‡
Phytotech, Inc., 1 Deer Park Drive, Suite I, Monmouth
Junction, New Jersey 08852, and Institute of Cell Biology and
Genetic Engineering, National Academy of Science, 148
Zabolotnogo Street, Kiev, 252143, Ukraine
Remediation of soil contaminated with 137Cs remains one
of the most challenging tasks after the Chernobyl 1986
accident. The objectives of this research were to (1) identify
extractants that may be used to solubilize 137Cs in soil
solution, (2) study the effect of soil amendments on 137Cs
accumulation by plants, and (3) evaluate the applicability of
phytoextraction for environmental restoration of soil
contaminated with 137Cs. The availability of 137Cs to the
plants in Chernobyl soil was limited, because this radionuclide
was tightly bound to exchange sites of soil particles or
incorporated into the crystalline structure of primary and
secondary minerals. Out of 20 soil amendments tested to
increase 137Cs desorption/solubility in the soil, ammonium
salts were found to be the most practical soil amendment
that can potentially increase 137Cs bioavailability. Among
the screened plants, Amaranth cultivars had the highest
137Cs accumulation. Three sequential crops of Indian mustard
grown in one vegetation season at the experimental plot
resulted in a small decrease of 137Cs specific activity within
the top 15 cm of soil. Further improvements are necessary
to make phytoremediation technology a feasible option
for restoration of 137Cs-contaminated territories.
Introduction
Radioactive contamination of the environment is a problem
humanity cannot afford to ignore. The total activity of all
radioactive material released in the Chernobyl Nuclear Power
Plant, Ukraine (ChNPP) accident is presently estimated to
have been 3.7 × 1018 (1) to 12 × 1018 Bq (2). The presence
of radionuclides in soil and water often jeopardizes ecosystem
stability and poses serious risk to human health (3, 4).
A variety of environmental restoration methods for
radioactively contaminated sites have been developed and
used with some success (5). However, these technologies
may be prohibitively costly if large areas of land or volumes
of water are involved. Hence, there is a great need for reliable
and inexpensive technologies that are capable of reducing
radiation to environmentally acceptable levels. Such tech-
* Corresponding author phone: (732) 438-0900 ext. 12; fax: (732)
438-1209; e-mail: DUSHENKOV@AOL.COM.
† Phytotech, Inc.
‡ Institute of Cell Biology and Genetic Engineering.
10.1021/es980788+ CCC: $18.00  1999 American Chemical Society
Published on Web 12/12/1998
nologies might also be effectively used in pollution prevention
and waste reduction programs.
Recently, significant attention has been drawn to phy-
toremediation, an emerging technology using plants to
remove pollutants from the environment. Phytoremediation
could provide an affordable way to restore the economical
value of contaminated land. This technology employs a
plant’s natural ability to concentrate essential and nones-
sential elements in their tissues. Plants are not capable of
distinguishing isotopes of the same element. Radioactive
isotopes such as 14C, 18O, 32P, 35S, 64Cu, and 59Fe are widely
used as a tracers in plant physiology and biochemistry. In
some cases, plants react analogously to ions with similar
physicochemical properties. It is known that Sr is an analogue
of Ca in living organisms (6), and the effect of K on 137Cs
accumulation in plants is well documented (7). The ability
of plants to tolerate elevated levels of heavy metals and to
accumulate them to unusually high levels has been shown
in a number of different plant species (8, 9). However, the
value of metal-accumulating plants for environmental
remediation has been fully realized only recently (10-13).
Several subsets of phytoremediation technology are being
developed (14). The most advanced are phytoextraction (15,
16)sthe use of metal-accumulating plants, which can
transport and concentrate metals from the soil in the roots
and above ground shoots; rhizofiltration (17)sthe use of plant
roots to absorb, concentrate, and precipitate toxic metals
from aqueous streams; and phytostabilizationsthe use of
plants to eliminate the bioavailability of toxic metals in soils.
The objectives of this research were to (1) identify extractants
that may be used to solubilize 137Cs in soil solution, (2) study
the effect of soil amendments on 137Cs accumulation by
plants, and (3) evaluate the applicability of phytoextraction
for environmental restoration of soil contaminated with 137Cs.
Materials and Methods
Extraction of 137Cs from Soil. Soil for this study was collected
from the top 15 cm at the experimental plot within the
Chernobyl Exclusion Zone in Chernobyl, Ukraine. The soil
was air-dried in the laboratory, sieved to 2 mm, mixed
thoroughly, and then analyzed for 137Cs activity. The soil was
classified as a sod podzolic with a loamy-sand texture derived
from sandy fluvio-glacial deposits. The soil had 2.5% organic
matter, pHKCl 5.5, and an electric conductivity at 0.20 dS m-1.
Solubilization of 137Cs from the Chernobyl soil was studied
in batch experiments. A soil sample of 133 g was placed in
a plastic bottle and then mixed with 1 L of a treatment
solution. These suspensions were sealed and placed on an
end-over-end shaker at room temperature for 24 h. The slurry
was filtered through cheesecloth filter, and the filtrate was
centrifuged at 2000 rpm for 12 min. The resulting supernatant
was used for 137Cs activity determination. Ammonium acetate
(0.1 M) was used to successively extract the soil sample with
gradually increasing equilibration times (1, 3, 7, and 14 days).
Three replicates were used for all treatments.
Different surfactants (Triton X-100, triethanolamine hy-
drochloride, hydroxylammine hydrochloride, sodium lauryl
sulfate, sodium laurate, Calgon), organic (oxalic acid, citric
acid) and inorganic (HCl, HNO3) acids, and salts with cations
similar to Cs in physicochemical properties (NH4C2H3O2,
NH4NO3, (NH4)2SO4, KNO3, K2SO4, CsNO3, KCl, RbCl, FeCl3‚
6H20) were used to desorb 137Cs from the soil. All chemicals
were obtained from Sigma, U.S.A.
Field Experiments. An experimental plot was established
on the heavily contaminated soil at the Northwest border of
Chernobyl, Ukraine, approximately 10 km south of the ChNPP
VOL. 33, NO. 3, 1999 / ENVIRONMENTAL SCIENCE & TECHNOLOGY 9 469
TABLE 1. Desorption of 137Cs from the Chernobyl Soila
concn of specific activity % of initial
treatment solution active ingredient (10-12 Ci L-1) activity removed
deionized water N/A 28 ( 6 0.3
Triton X-100 0.5% 28 ( 0.3 0.3
triethanolamine hydrochloride 1% 31 ( 3.6 0.3
hydroxylammine hydrochloride 0.1 M 41 ( 3.1 0.4
sodium lauryl sulfate 1% 53 ( 0.5 0.5
sodium laurate 1% 142 ( 6 1.3
oxalic acid 1M 144 ( 18 1.3
citric acid 1M 190 ( 9 1.8
sodium lauryl sulfate, citric acid 1%, 1M 195 ( 11 1.8
hydrochloric acid 1.0 N 268 ( 17 2.5
ammonium acetate 0.1 M 435 ( 66 4.1
calgon 1% 463 ( 13 4.3
ammonium nitrate 0.1 N 492 ( 13 4.6
potassium sulfate 0.1 M 496 ( 21 4.6
cesium nitrate 0.01 M 530 ( 12 5.0
potassium nitrate 0.5 N 615 ( 63 5.7
hydrochloric acid, potassium cloride, ferric chloride 0.1 M each 733 ( 31 6.9
ammonium sulfate 0.1 M 909 ( 25 8.5
rubidium chloride 1M 1170 ( 67 10.9
nitric acid 5M 2220 ( 9 20.7
a A soil sample of 133 g was placed in a plastic bottle and mixed with 1 L of a treatment solution. The bottles with the soil/extractant suspension

were sealed and placed on an end-over-end shaker at room temperature for 24 h. The slurry was filtered through cheesecloth filter, and the filtrate
was centrifuged at 2000 rpm for 12 min. Average ( standard deviation of three replicates is shown in the table.

fourth reactor that was damaged in 1986. The soil within the
plot was classified as a sod podzolic with a loamy-sand texture
derived from sandy fluvio-glacial deposits. The soil had pHKCl
of 5.5, 2.5% organic matter content, and electric conductivity
of 0.20 dS m-1. Soil fertility was characterized by nitrogen
(N) 96 kg ha-1, phosphorus (P2O5) 30 kg ha-1, potassium 28
kg ha-1, Mn 29.1 mg kg-1, Cu 1.4 mg kg-1, and Zn 3.3 mg kg-1.
To improve soil fertility at the experimental plot, lime (5000
kg ha-1), ammonium nitrate (100 kg ha-1), triple super
phosphate (288 kg ha-1), potassium chloride (190 kg ha-1),
and ammonium sulfate (190 kg ha-1) were applied to the soil
surface and incorporated to a depth of 15 cm prior to planting.
The bioaccumulation coefficient, calculated as a ratio of 137Cs
specific activity in the plant versus 137Cs specific activity in
the soil, was used to evaluate 137Cs phytoextraction.
Screening of Plants for 137Cs Accumulation. A portion of
the experimental plot was subdivided into 2 m × 2 m blocks
with 1 m borders and was used to screen high biomass crops
for 137Cs accumulation. A variety of Amaranth species
(Amaranthus bicolor L., A. caudatus L., A. cruentus L., A.
hybridus L., A. retroflexus L.), Indian mustard (Brassica juncea
(L.) Czern.), corn (Zea mays L.), peas (Pisum sativum L.),
Jerusalem artichoke (Helianthus tuberosus L.), sunflower
(Helianthus annuus L.), and sunflower x Jerusalem artichoke
hybrid (H. tuberosus L. x H. annuus L.) were used in the
screening. Plants were seeded by hand in rows and were
weeded and watered as needed. After 9 weeks, plants were
harvested, air-dried, and analyzed for 137Cs activity.
137Cs Compartmentalization in Plants. To study the
radiocesium distribution within the plant, in addition to
harvesting above-ground parts, the roots of corn, sunflower,
and Indian mustard were dug out, washed in tap water, air-
dried, and analyzed for 137Cs activity.
Impact of Soil Amendments on 137Cs Accumulation by
Plants. A portion of the experimental plot was subdivided
into 2 m × 2 m blocks with 1 m borders and was used to
evaluate the effect of soil amendments on 137Cs accumulation
by plants in their above-ground biomass. Triplicates were
used in each treatment. Soil amendments were applied either
before planting, when no plant toxicity was expected, or 1
week before harvest, when the amendments may interfere
with plant growth. To the plots with Indian mustard and
sunflower, the following amendments were added: (a) excess
of potassium (incorporated to the soil before planting at the
rate of KCl - 1150 kg ha-1 and KNO3 3000 kg ha-1); (b)
potassium salt of DTPA (diethylenetrinitrilopentaacetic acid,
0.5 M solution sprayed on the soil surface 1 week before
harvesting at the rate 1 L m-2); (c) potassium salt of EDTA
(ethylenedinitrilotetraacetic acid, 0.5 M solution sprayed on
the soil surface 1 week before harvesting at the rate 1 L m-2);
and (d) biogumus (organic fertilizer, incorporated to the soil
before planting at the rate 6250 kg ha-1). The effect of NH4+
on 137Cs accumulation in plants was also tested on A.
retroflexus cv. myronivka. One week before harvest (NH4)2SO4
or NH4NO3 was applied to the test plots as a water solution
at the rate of 1500 kg ha-1.
Phytoextraction Field Experiment. A 40 m2 plot was
established for the phytoextraction (defined as the removal
of metals from soil by plants) trial. Soil was tilled to 15 cm
depth. Indian mustard was planted by hand in rows spaced
12.5 cm apart at a depth of 1.5 cm. A press wheel was used
to firm the soil around the seed. After 6 weeks, all above-
ground biomass was harvested, and the plot was then tilled
and replanted. Three sequential Indian mustard crops were
grown during one vegetation period. Ammonium nitrate (50
kg ha-1), triple super phosphate (144 kg ha-1), potassium
chloride (100 kg ha-1), and ammonium sulfate (100 kg ha-1)
were applied to the soil surface and incorporated to a depth
of 15 cm prior to planting the second and third crops. The
specific activity of 137Cs was measured at 14 sampling points
in the soil at the beginning of the experiment and in the soil
and plants after each crop. All harvested biomass was
removed from the plot.
Determination of Radionuclides. Soil and plant samples
were air-dried prior to analyses. Plants were cut to <2 cm.
The activity of 137Cs in the soil and plants was determined
directly by gamma-spectrometry using a HPGe detector,
coupled to a multichannel. The efficiency of the system was
30% as determined with a 152Eu standard source. The systems
were calibrated with soils and plant material containing
known amounts of 137Cs in appropriate standard containers.
All results were decay corrected to May 1, 1996.
Statistical Procedures. All experiments were done at least
in three replicates. All data were subject to ANOVA. Fisher’s
least significant test (P < 0.05) was used to evaluate differences
between treatments and changes in 137Cs activity in soil

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FIGURE 1. Sequential desorption of 137Cs from the Chernobyl soil
with ammonium acetate (0.1 M). A soil sample of 133 g was placed
in a plastic bottle and then mixed with 1 L of a treatment solution.
The bottles with the soil/extractant suspension were sealed and
placed on an end-over-end shaker at room temperature for 1, 3, 7,
and 14 days, respectively. After the equilibration, the slurry was
filtered through cheesecloth filter, and the filtrate was centrifuged
at 2000 rpm for 12 min. The resulting supernatant was used for 137Cs
activity determination. Remaining soil was used for sequential
extraction.
following phytoremediation. The soil surface maps were
produced using Surfer 6.04 software (Golden Software, Inc.)
and were based on linear kriging of sampling points data.
Results
(Table 1). Only a small fraction (<0.3%) of 137Cs was water
soluble. The majority of the surfactants tested did not affect
137
Cs desorption greatly (<2.0%). Organic acids were also
ineffective in mobilizing 137Cs into solution. Even application
of 5 M nitric acid resulted in the extraction of only 20.7% of
radiocesium from the soil. Ammonium, potassium, and
rubidium salts demonstrated a propensity to enhance Cs
desorption from the soil. Stable Cs isotope was also effective
in replacing radiocesium from the binding sites.
Ammonium acetate (0.1 M) was used for four successive
extractions with gradually increasing time of equilibration.
Almost half of the 137Cs removed from the soil sample during
the experiment was extracted at the first equilibration (1
day) of the soil/extractant suspension. Effectiveness of
extraction was significantly reduced with the number of
extractions (Figure 1).
Screening of Plants for the 137Cs Accumulation. Sixteen
high biomass cultivars of 10 species were screened for 137Cs
accumulation. Indian mustard, a common plant for reme-
diation of Pb-contaminated soils, had the lowest yield among
the tested cultivars. A large group of plants, including the
majority of the Amaranth cultivars, peas, and sunflower, had
an overall yield close to 500 g of dried biomass per m2 (Figure
2). Cesium-137 specific activity within this group of species
ranged from several hundred Bq kg-1 in peas and sunflower
up to 3000 Bq kg-1 for A. retroflexus cv. belozernii. Another
group of cultivars that included corn, Jerusalem artichoke,
and sunflower x Jerusalem artichoke hybrid had a high yield
in conjunction with relatively low 137Cs accumulation.
Amaranthus retroflexus cvs. aureus and PT-95 were the
leading cultivars in total radioactivity removal from the soil
(Table 2). These cultivars combined high biomass production
with the high level of 137Cs accumulation in the above-ground
biomass.
137Cs Compartmentalization in Plants. Radiocesium

Extraction of 137Cs from Soil. Radiocesium (137Cs) was compartmentalization within the plant was studied in corn,
strongly adsorbed by soil particles and was difficult to extract sunflower, and Indian mustard. Roots of these species had

FIGURE 2. Screening results. Yield and 137Cs activity in shoots. Plants were grown at the experimental plot at the Northwest border of
Chernobyl, Ukraine, approximately 10 km south of the ChNPP fourth reactor that was damaged in 1986. Aa - Amaranthus retroflexus L.
cv. aureus; Ab - Amaranthus retroflexus L. cv. belozernii; Abi - Amaranthus bicolor L.; Ac - Amaranthus cruentus L.; Acu - Amaranthus
caudatus L.; Ah - Amaranthus hybridus L.; Am - Amaranthus cruentus L. cv. myronivka; Ap - Amaranthus cruentus L. cv. paniculatus;
Ar - Amaranthus retroflexus L. cv. PT - 95; Ara - Amaranthus retroflexus L. cv. Antey; Bj - Brassica juncea (L.) Czern.; Ha - Helianthus
annuus L.; Ht - Helianthus tuberosus L.; Hta - Helianthus tuberosum L. x Helianthus annuus L.; Ps - Pisum sativum L.; Zm - Zea mays
L.

VOL. 33, NO. 3, 1999 / ENVIRONMENTAL SCIENCE & TECHNOLOGY 9 471

TABLE 2. Bioaccumulation Coefficient and Total 137Cs Removal from Soila
bioaccumulation total
species and cultivars coeff removal (Bq m-2)
Amaranthus retroflexus L. cv. PT-95 1.50 3225
Amaranthus retroflexus L. cv. aureus 1.90 2440
Amaranthus retroflexus L. cv. belozernii 1.41 1392
Amaranthus cruentus L. 1.32 1251
Helianthus tuberosum L. x Helianthus annuus L. 0.49 1221
Amaranthus caudatus L. 2.03 1144
Amaranthus cruentus L. cv. myronivka 1.07 1053
Helianthus tuberosus L. 0.30 846
Amaranthus hybridus L. 0.60 719
Amaranthus retroflexus L. cv. Antey 1.07 641
Amaranthus bicolor L. 0.59 417
Amaranthus cruentus L. cv. paniculatus 0.53 412
Zea mays L. 0.28 409
Helianthus annuus L. 0.24 319
Pisum sativum L. 0.48 244
Brassica juncea (L.) Czern. 0.47 194
a Plants were grown at the experimental plot at the Northwest border of Chernobyl, Ukraine, approximately 10 km south of the ChNPP fourth

reactor that was damaged in 1986. Bioaccumulation coefficient was calculated as a ratio of 137Cs specific activity in the plant versus 137Cs specific
activity in the soil.

FIGURE 4. Effect of soil amendments on 137Cs accumulation in Indian

FIGURE 3. Radiocesium specific activity in above-ground and
underground parts of selected plants. Shoots were harvested 2 cm
above ground, air-dried, and analyzed for 137Cs activity. Roots were
dug out, washed in tap water, air-dried, and analyzed for 137Cs
activity.
2.5-3.4 times greater 137Cs activity compared to the above-
ground parts (Figure 3). A positive correlation was found
between 137Cs activity in the roots and 137Cs activity in the
shoots.
Impact of Soil Amendments on 137Cs Accumulation by
Plants. A number of soil amendments including the addition
of exchange ions, chelating agents, and organic matter were
tested for further influence on 137Cs accumulation in plants.
Biogumus, EDTA, and DTPA did not significantly affect the
accumulation of 137Cs by Indian mustard. However, the
introduction of potassium into the soil as 1150 kg ha-1 KCl
coupled with 3000 kg ha-1 KNO3, resulted in a slightly greater
bioaccumulation coefficient compared to the control and
mustard (B. juncea) and sunflower (H. annuus). Triplicates were
used in each treatment. The following amendments were added:
K+ - an excess of potassium, incorporated to the soil before planting
at the rate KCl - 1150 kg ha-1 and KNO3 3000 kg ha-1; DTPA -
potassium salt of DTPA, diethylenetrinitrilopentaacetic acid, 0.5 M
solution sprayed on the soil surface 1 week before harvesting at
the rate 1 L m-2, EDTA - potassium salt of EDTA, ethylenedini-
trilotetraacetic acid, 0.5 M solution sprayed on the soil surface 1
week before harvesting at the rate 1 L m-2; and Biogumus - organic
fertilizer, incorporated to the soil before planting at the rate 6250
kg ha-1.
other treatments (Figure 4). Sunflower generally had lower
bioaccumulation coefficients than Indian mustard. Biogumus
and chelating agents did not dramatically affect 137Cs
accumulation in sunflowers (Figure 4). Similarly, no statisti-
cally significant difference in 137Cs accumulation in Amaranth
was observed at the levels of ammonium salts soil amend-
ment used for this experiment (Figure 5). However, incor-
porating 1500 kg (NH4)2SO4 per ha resulted in a slight increase
in the average bioaccumulation coefficient.

472 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 33, NO. 3, 1999


FIGURE 5. Effect of ammonium soil amendments on 137Cs ac-
cumulation in Amaranth (A. retroflexus cv. myronivka). Ammonium
sulfate or ammonium nitrate was applied to the test plots as a
water solution at the rate of 1500 kg ha-1 1 week before harvest.
FIGURE 6. Radiocesium activity in Indian mustard shoots versus
radiocesium activity in soil.
Phytoextraction Field Experiment. Radiocesium activity
in the soil and the corresponding plants was measured for
each of three Indian mustard crops at 14 sampling points.
Significant variability of 137Cs concentrations in the plants
and soil was observed. Nevertheless, a positive linear
correlation for 137Cs specific activity in the soil and in the
plants was established (Figure 6).
There was a general trend for 137Cs in soil to decline,
starting at an average of 2558 Bq kg-1 in spring and gradually
dropping to an average of 2239 Bq kg-1 after the harvest of
third crop. Although, the difference between means of 137Cs
specific activity in soil measured at the beginning of the
experiments and measured after each crop was not statisti-
cally significant at P < 0.05, visible changes in the 137Cs surface
distribution were found (Figure 7). Areas having 137Cs levels
>3000 Bq kg-1 shrank from 29.4% of the total plot area before
treatment to 7.7% after treatment. After the final harvest of
the phytoremediation crop, areas having 137Cs levels <2000
Bq kg-1 increased to 33.3% compared to 27.4% before
treatment.
Discussion
The laboratory and field experiments demonstrated that
plants may be used to remove 137Cs from soil contaminated
with radionuclides during the Chernobyl Nuclear Power Plant
accident in 1986. It was shown that plants significantly differ
in their ability to accumulate 137Cs. Additions of soil amend-
ments to help mobilize 137Cs from soil particles may increase
137
Cs accumulation by the plants; however, our study
uncovered that phytoremediation of 137Cs in the Chernobyl
region has certain limitations.
The experimental plot was located in the area contami-
nated with 137Cs from the ChNPP accident in 1986. Radioactive
aerosols deposited on the soil surface during the accident
had a heterogeneous structure (18). Radiocesium was partially
associated with coarse and fine dispersed fragments of
irradiated fuel having a mixed uranium oxide core (fuel type
of deposition). Another type of aerosol consisted of a core,
covered by recondensed cesium (condensed type of fallout).
Both types of radiocesium deposition to the soil contributed
evenly to the contamination of the experimental plot (19).
Field observations showed that the majority of the 137Cs
remained in the top 5 cm of the soil (20) several years after
deposition. It is generally accepted that condensed radio-
nuclides migrate faster than radionuclides from fuel type of
deposition (1). However, a migration of the 137Cs to the deeper
soil layers is a very slow process (21), and the velocity of 137Cs
vertical migration usually remains sufficiently below 1 cm
year-1 (22). A long-term restraining of surface deposited 137Cs
within the rooting zone (top 0-15 cm) is an important
precondition for effective phytoremediation.
The accumulation of 137Cs in plants is a complex process
that is determined by an interaction of numerous factors
(23). Soil type and soil physicochemical properties (18, 24,
25), timing from the 137Cs deposition (25, 26), type of
radionuclide deposition (18), and plant species physiology
(27) are among the major factors affecting radiocesium
accumulation in plants. In this study, a combination of soil
properties and aging time determined the behavior of 137Cs
in the soil and its potential bioavailability. Radiocesium
speciation in the soil during the 10 years after the Chernobyl
accident was affected by radionuclide release from the fuel
particles and its incorporation into soil phases. Weathering
and chemical leaching of the fuel particles under the natural
conditions released 137Cs in the soil solution. It has been
shown that soil microorganisms and root exudates may play
important roles in accelerating the destruction of fuel particles
(28). Once released, radiocesium ions moved to exchange
sites of soil particles or were incorporated into the crystalline
structure of primary and secondary minerals. Kinetics of the
137Cs bounding to the soil matrix prevail the release from the
fuel particles. The overall rate constant for cesium fixation
in the sod podzolic soil was estimated at about 8 × 10-4
day-1 (19). By the time of the phytoremediation experiments
in 1996, the majority of the 137Cs was tightly fixed in the soil
with a diminutive portion of total 137Cs in the soil solution,
and only about 10% was potentially bioavailable (extractable
and labile fractions) (19). Agapkina with colleagues (29) found
that a significant amount of 137Cs in the soil solution in the
upper layer of the forest soil was associated with organic
matter, evenly distributed across fractions with different
molecular weight. Consequently, bounding with organic
matter may also affect 137Cs accumulation by plants.
Ploughing leads to a more even redistribution of the
radionuclide contaminants through the soil profile, thus
reducing the 137Cs concentration in the top 0-5 cm layer (1,
VOL. 33, NO. 3, 1999 / ENVIRONMENTAL SCIENCE & TECHNOLOGY 9 473
FIGURE 7. Top 15 cm 137Cs distribution at 40 m2 (5 m × 8 m) phytoextraction experimental plot at Chernobyl. Soil was tilled to 15 cm depth.
Indian mustard was planted by hand in rows spaced 12.5 cm apart at a depth of 1.5 cm. A press wheel was used to firm the soil around
the seed. After 6 weeks all above-ground biomass was harvested, and the plot was tilled and replanted. Three sequential Indian mustard
crops were grown during one vegetation period. Radiocesium specific activity was measured at 14 sampling points in soil at the beginning
of the experiment and in the soil and plants after each crop. Maps were produced using Surfer 6.04 software (Golden Software, Inc.) and
were based on linear kriging of 14 sampling points.
30). Ploughing is also usually associated with a significant
reduction in 137Cs accumulation by plants (26).
In general, 137Cs bioavailability to plants was relatively
higher in the Chernobyl region during the first two years
after the accident (25) and sharply declined afterward. Low
bioavailability of radiocesium in the Chernobyl soil may
significantly limit 137Cs accumulation by roots. It was shown
that 137Cs accumulation by plants is determined by the
content of exchangeable and mobile forms of radionuclide
in the soil (18). Soil amendments are widely used in the
phytoremediation technology to increase bioavailability and
enhance accumulation of heavy metals (31) and radionuclides
(13) in plants. In a search for a potential soil amendment,
we screened 20 different chemicals and their combinations
for the ability to desorb 137Cs from soil. It is generally agreed
that K+, NH4+, Rb+, and Cs+ form a homologous series of
ions with considerable physicochemical similarity. In coher-
ence with previous studies (32), it was found that the addition
of monovalent cations similar to Cs+ physicochemical
properties resulted in the most significant levels of 137Cs
desorption from the Chernobyl soil. In our experiments,
ammonium was superior to potassium for displacing 137Cs
from bounding sites and releasing 137Cs into solution.
Therefore, ammonium salts were selected as the primary
soil amendment for the field experiments. In the pot
experiments, treatment of soil with ammonium nitrate
stimulated 137Cs accumulation in the above-ground biomass
(32); however, in the field experiments, the addition of
ammonium salts to the soil did not affect 137Cs accumulation
by plants (33) (Figure 5). Failure to increase 137Cs accumula-
tion by plants in the field experiments may be partially
attributed to a relatively lower amount of NH4+ introduced
to the soil in the field experiments. It is also probable that
NH4+ cations not only helped to release 137Cs in the soil
solution but also competed with cesium cations for plant
uptake.
Even though the high biaccumulation ratio for Cs was
reported in earlier hydroponic experiments (32, 34), radio-
cesium activity in the shoots of the plants grown in 137Cs-
contaminated areas were usually significantly lower than in
the soil (23, 35). Our data showed that radiocesium con-
centration in the roots was about four times higher than the
radiocesium concentration in the shoots (Figure 3). These
data correlated well with other results obtained hydroponi-
474 9 ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 33, NO. 3, 1999
cally (34) and suggests that for effective phytoremediation
of 137Cs it is necessary to induce radionuclide transport to
the above-ground parts.
The ability of plant species to accumulate 137Cs in the
above-ground parts may differ by an order of magnitude
(27). The difference in 137Cs accumulation varied from 2-4-
fold within cereals and reached 27-fold for all field crops
(26). Significant variation in radiocesium accumulation was
observed in the cultivars of the same species (Figure 2). We
found Amaranthus species A. cruentus, A. retroflexus, and A
caudatus were able to concentrate radiocesium in the above-
ground parts. Lasat et al. (33) reported a bioaccumulation
coefficient of >2 for A. retroflexus grown on a 137Cs-
contaminated soil at Brookhaven National Laboratory, U.S.A.
These data compared favorably to the biaccumulation
coefficients of <1 for Indian mustard and tepary bean
(Phaseolus acutifolius A. Gray) at the same plot (33). In the
laboratory experiments, with readily available 137Cs in sph-
agnum moss/perlite growth medium, a bioaccumulation
coefficient close to one was obtained in Ponderosa and
Monterey pine seedlings (36).
The developmental stage of the plant may also play an
important role in radionuclide accumulation. In laboratory
experiments (34), radiocesium shoot concentration followed
changes in K concentrations during plant development.
Radiocesium content rapidly increased between 11 and 28
days after sowing and reached a maximum at 35 days. After
that, a slight decrease in concentration was observed.
Light sandy soils are characterized by relatively high level
of available forms compared to heavy clay soils for 137Cs.
Overall, the accumulation of 137Cs in plants dropped 2-3
times over 7 years after the Chernobyl accident (26). The
residence half-time of the 137Cs content in grassland plants
was observed to be 2.0-2.2 years for the initial period after
the accident and increased to 4-12 years in following period
(26). Phytoremediation has the greatest potential as a land
restoration technology for 137Cs-contaminated areas during
the first few years after radionuclide deposition, when 137Cs
remains bioavailable.
For successful restoration of radioactively contaminated
territories, it is crucially important that plants be able to
remove a significant portion of radioactivity from the soil.
In addition to high biomass production, a potential phy-
toremediation crop should have the ability to accumulate
 radionuclide in the above-ground parts to the concentration
exceeding the soil concentration (i.e. bioaccumulation coef-
ficient >1). A major obstacle limiting phytoremediation of
137Cs is that after deposition, 137Cs is rapidly incorporated
into soil clay minerals and becomes unavailable for plants.
Currently, phytoremediation at Chernobyl may target only
the bioavailable 137Cs which represent 10-25% of the total
137
Cs. Phytoremediation may be a valuable option during
the first years after 137Cs deposition, providing cultivars with
high bioaccumulation coefficients will be found and/or
mechanisms for inducing 137Cs translocation from the roots
to the shoots will be discovered.
Acknowledgments
The authors thank the Administration of the Chernobyl
Exclusion Zone for valuable assistance and Dr. Mark Elless
for his critical review. The authors also thank Ms. Kathy
Makowski for her assistance in manuscript preparation.
Literature Cited
(1) Askbrant, S.; Melin, J.; Sandalls, J.; Rauret, G.; Vallejo, R.; Hinton,
T.; Cremers, A.; Vandecastelle, C.; Lewyckyj, N.; Ivanov, I. A.;
Firsakova, S. K.; Arkhipov, N. P.; Alexakhin, R. M. J. Environ.
Radioactivity 1996, 31, 287-312.
(2) IAEA International Conference on One Decade After Cherno-
byl: Summing Up the Consequences of the Accident jointly
sponsored by the European Commission, International Atomic
Energy Agency, World Health Organization, in cooperation with
the United Nations (Department of Humanitarian Affairs),
Vienna, Austria, 1996; 555.
(3) Prohl, G.; Muller, H. Radiat. Environ. Biophys. 1996, 35, 205-
218.
(4) Eisenbud, M. The human environment - past, present and future;
National Council on Radiation Protection and Measurements:
Bethesda, MD, 1983.
(5) Laraia, M. In Planning for environmental restoration of rado-
actively contaminated sites in Central and Eastern Europe;
IAEA: Viena, 1996; Vol. 3.
(6) Kabata-Pendias, A.; Pendias, H. Trace elements in soils and plants;
CRC Press: Boca Raton, FL, 1989.
(7) Seel, J. F.; Whicker, F. W.; Adriano, D. C. Health Phys. 1995, 68,
793-799.
(8) Ernst, W. H. O.; Verkleij, J. A. C.; Schat, H. Acta Bot. Neerl 1992,
41, 229-248.
(9) Baker, A. J. M.; Brooks, R. R. Biorecovery 1989, 81-126.
(10) Raskin, I.; Smith, R. D.; Salt, D. E. Curr. Opin. Biotechnol. 1997,
8, 221-226.
(11) Raskin, I.; Kumar, P. B. A. N.; Dushenkov, S.; Salt, D. Curr. Opin.
Biotechnol. 1994, 285-290.
(12) Cunningham, S. D.; Ow, D. W. Plant. Physiol. 1996, 110, 715-
719.
(13) Huang, J. W.; Blaylock, M. J.; Kapulnik, Y.; Ensley, B. D. Environ.
Sci. Technol. 1998, 32, 2004-2008.
(14) Salt, D. E.; Blaylock, M.; Kumar, N. P. B. A.; Dushenkov, V.;
Ensley, B. D.; Chet, I.; Raskin, I. Biotech. 1995, 13, 468-474.
View publication stats
(15) Kumar, N. P. B. A.; Dushenkov, V.; Motto, H.; Raskin, I. Environ.
Sci. Technol. 1995, 29, 1232-1238.
(16) Dushenkov, S.; Kapulnik, Y.; Blaylock, M.; Sorochinsky, B.;
Raskin, I.; Ensley, B. In Global Environmental Biotechnology;
Wise, D. L., Ed.; Elsevier Science B. V.: Amsterdam, 1997.
(17) Dushenkov, V.; Kumar, N. P. B. A.; Motto, H.; Raskin, I. Environ.
Sci. Technol. 1995, 29, 1239-1245.
(18) Fesenko, S. V.; Spiridonov, S. I.; Sanzharova, N. I.; Alexakhin,
R. M. J. Environ. Radioactivity 1997, 34, 287-313.
(19) Krouglov, S. V.; Kurinov, A. D.; Alexakhin, R. M. J. Environ.
Radioactivity 1998, 38, 59-79.
(20) Knatko, V. A.; Skomorokhov, A. G.; Asimova, V. D.; Strakh, L. I.;
Bogdanov, A. P.; Mironov, V. P. J. Environ. Radioactivity 1996,
30, 185-196.
(21) Ivanov, Y. A.; Lewyckyj, N.; Levchuk, S. E.; Prister, B. S.; Firsakova,
S. K.; Archipov, N. P.; Archipov, A. N.; Kruglov, S. V.; Alexakhin,
R. M.; Sandalls, J.; Askbrant, S. J. Environ. Radioactivity 1997,
35, 1-21.
(22) Arapis, G.; Petrayev, E.; Shagalova, E.; Zhukova, O.; Sokolik, G.;
Ivanova, T. J. Environ. Radioactivity 1997, 34, 171-185.
(23) Askbrant, S.; Sandalls, J. J. Environ. Radioactivity 1998, 38, 85-
95.
(24) Roca, M. C.; Vallejo, V. R.; Roig, M.; Tent, J.; Vidal, M.; Rauret,
G. J. Environ. Qual. 1997, 26, 1354-1362.
(25) Krouglov, S. V.; Filipas, A. S.; Alexakhin, R. M.; Arkhipov, N. P.
J. Environ. Radioactivity 1997, 34, 267-286.
(26) Sanzharova, N. I.; Fesenko, S. F.; Lisyanskii, K. B.; Kuznetsov,
V. K.; Abramova, T. N.; Kotik, V. A. Pochvodenie 1997, 159-164
(in Russian).
(27) Grodzinsky, D. M.; Kolomiets, K. D.; Kutlahmedov, Y. A.; Bulah,
A. A.; Dmitriev, A. P.; Homlyak, M. N.; Bubryak, I. I.; Zezina, N.
B.; Mikheev, A. N.; Kravets, A. P. Antropogenouse radionuclide
anomaly and plants; Lybid′: Kiev, 1991.
(28) Kravets, A. P.; Grodzinsky, D. M.; Pavlenko, Y. A.; Zhdanova, N.
N.; Vasilevskaya, A. I.; Sinyavskaya, O. I. Radiat. Biol. Ecol. 1993,
33, 93-98.
(29) Agapkina, G. I.; Tikhomirov, F. A.; Scheglov, A. I. J. Environ.
Radioactivity 1995, 29, 257-269.
(30) Salbu, B.; Oughton, D. H.; Ratnikov, A. V.; Zhigareva, T. L.;
Kruglov, S. V.; Petrov, K. V.; Grebenshakikova, N. V.; Firsakova,
S. K.; Astasheva, N. P.; Loshchilov, N. A.; Hove, K.; Strand, P.
Health Physics 1994, 67, 518-528.
(31) Blaylock, M. J.; Salt, D. E.; Dushenkov, S.; Zakharova, O.;
Gussman, C.; Kapulnik, Y.; Ensley, B. D.; Raskin, I. Environ. Sci.
Technol. 1997, 31, 860-865.
(32) Lasat, M. M.; Norvell, W. A.; Kochian, L. V. Plant Soil 1997, 195,
99-106.
(33) Lasat, M. M.; Fuhrmann, M.; Ebbs, S. D.; Cornish, J. E.; Kochian,
L. V. J. Environ. Qual. 1998, 27, 165-169.
(34) Smolders, E.; Shaw, G. Plant Soil 1995, 176, 1-6.
(35) Cline, J. F.; Rickard, W. H. Health Physics 1972, 23, 317-324.
(36) Entry, J. A.; Rygiewicz, P. T.; Emmingham, W. H. J. Environ.
Qual. 1993, 22, 742-746.
Received for review July 31, 1998. Revised manuscript re-
ceived October 20, 1998. Accepted October 29, 1998.
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